Dataset Information

Meaning in the avian auditory cortex: neural representation of communication calls.

ABSTRACT: Understanding how the brain extracts the behavioral meaning carried by specific vocalization types that can be emitted by various vocalizers and in different conditions is a central question in auditory research. This semantic categorization is a fundamental process required for acoustic communication, and presupposes discriminative and invariance properties of the auditory system for conspecific vocalizations. Songbirds have been used extensively to study vocal learning, but the communicative function of all their vocalizations and their neural representation has yet to be examined. In this study, we first generated a library containing almost the entire zebra finch vocal repertoire, and organised communication calls along nine different categories according to their behavioral meaning. We then investigated the neural representations of these semantic categories in the primary and secondary auditory areas of six anesthetised zebra finches. To analyse how single units encode these call categories, we described neural responses in terms of their discrimination, selectivity and invariance properties. Quantitative measures for these neural properties were obtained with an optimal decoder using both spike counts and spike patterns. Information theoretic metrics show that almost half of the single units encode semantic information. Neurons achieve higher discrimination of these semantic categories by being more selective and more invariant. These results demonstrate that computations necessary for semantic categorization of meaningful vocalizations are already present in the auditory cortex, and emphasise the value of a neuro-ethological approach to understand vocal communication.

SUBMITTER: Elie JE

PROVIDER: S-EPMC4347984 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Publications

Meaning in the avian auditory cortex: neural representation of communication calls.

Elie Julie E JE Theunissen Frédéric E FE

The European journal of neuroscience 20150301 5

Understanding how the brain extracts the behavioral meaning carried by specific vocalization types that can be emitted by various vocalizers and in different conditions is a central question in auditory research. This semantic categorization is a fundamental process required for acoustic communication, and presupposes discriminative and invariance properties of the auditory system for conspecific vocalizations. Songbirds have been used extensively to study vocal learning, but the communicative f ...[more]

PMID: 25728175

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Project description:One of the most complex tasks performed by sensory systems is "scene analysis": the interpretation of complex signals as behaviorally relevant objects. The study of this problem, universal to species and sensory modalities, is particularly challenging in audition, where sounds from various sources and localizations, degraded by propagation through the environment, sum to form a single acoustical signal. Here we investigated in a songbird model, the zebra finch, the neural substrate for ranging and identifying a single source. We relied on ecologically and behaviorally relevant stimuli, contact calls, to investigate the neural discrimination of individual vocal signature as well as sound source distance when calls have been degraded through propagation in a natural environment. Performing electrophysiological recordings in anesthetized birds, we found neurons in the auditory forebrain that discriminate individual vocal signatures despite long-range degradation, as well as neurons discriminating propagation distance, with varying degrees of multiplexing between both information types. Moreover, the neural discrimination performance of individual identity was not affected by propagation-induced degradation beyond what was induced by the decreased intensity. For the first time, neurons with distance-invariant identity discrimination properties as well as distance-discriminant neurons are revealed in the avian auditory cortex. Because these neurons were recorded in animals that had prior experience neither with the vocalizers of the stimuli nor with long-range propagation of calls, we suggest that this neural population is part of a general-purpose system for vocalizer discrimination and ranging.SIGNIFICANCE STATEMENT Understanding how the brain makes sense of the multitude of stimuli that it continually receives in natural conditions is a challenge for scientists. Here we provide a new understanding of how the auditory system extracts behaviorally relevant information, the vocalizer identity and its distance to the listener, from acoustic signals that have been degraded by long-range propagation in natural conditions. We show, for the first time, that single neurons, in the auditory cortex of zebra finches, are capable of discriminating the individual identity and sound source distance in conspecific communication calls. The discrimination of identity in propagated calls relies on a neural coding that is robust to intensity changes, signals' quality, and decreases in the signal-to-noise ratio.

Dataset Information

Meaning in the avian auditory cortex: neural representation of communication calls.

Publications

Meaning in the avian auditory cortex: neural representation of communication calls.

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